Evolution of Secondary Plant Metabolism

Abstract

The biosynthesis of secondary metabolites (SMs), which are important for the fitness of the plants as defence against herbivores
and microbes and also as signal compounds to attract pollinators and fruit dispersers, occurs universally in higher plants
and shows very high structural diversity. The evolution of SMs in higher plants rests on variation in the enzymatic manipulation
of a relatively small number of primary precursors. Evidence is presented that at least some of the genes encoding key enzymes
of biosynthesis probably have reached plants by ancient horizontal gene transfer (HGT), for example, from protobacteria or
cyanobacteria which later became mitochondria and plastids. Another source of SMs can be ectomycorrhizal and endophytic fungi;
they can directly provide plants with defence compounds or might have transferred their pathway genes into the genome of their
host plants times ago.

Key Concepts

Plants have evolved secondary metabolites as bioactive substances as a measure to protect themselves against herbivores.

Secondary metabolites are part of the innate immune system of plants, used to defend themselves against bacteria, fungi and
viruses.

Secondary metabolism is dynamic and can react in case of a herbivoral or microbial attack by activating prodrugs, by either
increasing the concentration of existing SM or by inducing the synthesis of new SMs (phytoalexins).

Secondary metabolites occur in a broad diversity and functionality.

Secondary metabolites derive from primary metabolites using a limited number of key pathways. Functional diversity is gained
by adding diverse combinations of reactive functional groups.

Terpenoids and phenolics are present in almost all plants, whereas alkaloids and other nitrogen‐containing SMs are more common
in angiosperms.

Some groups of SMs occur in a few restricted plant genera only, which are often not related.

The patchy distribution can be due to convergent evolution of the corresponding pathways.

Alternatively, the genes for SM biosynthesis have been introduced into the plant genome by horizontal gene transfer from protobacteria
(which became mitochondria) and cyanobacteria (which became chloroplast).

Some SMs are produced by endophytic fungi, which infect a limited number of often unrelated species. As a consequence, this
can also lead to a patchy distribution of SMs.

Figure 1. The evolution of five different classes of alkaloids from a common amino acid precursor, tyrosine. A given symbol always indicates the same carbon throughout the reaction scheme.

Figure 2. Distribution of 1‐btiq alkaloids in angiosperms mapped on a phylogenetic framework (APG II). Branches in which 1‐btiq are produced are printed in black and bold.

Figure 3. Distribution of quinolizidine alkaloid (QA) and pyrrolizidine alkaloids (PAs) in angiosperms mapped on a phylogenetic framework (APG II). Branches in which QA are produced are printed in blue, those with /PA in red.